Dual inhibitors of P-glycoprotein and tumor cell growth: (Re)discovering thioxanthones

Biochemical Pharmacology

Volumn 83, Issue 1, 2012, Pages 57-68

  Palmeira, Andreia ^a   Vasconcelos, M Helena ^a   Paiva, Ana ^a   Fernandes, Miguel X ^b   Pinto, Madalena ^a   Sousa, Emília ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF MADEIRA   (Portugal)

Author keywords

Anticancer; Dual ligands; Multidrug resistance; P glycoprotein; Thioxanthones

Indexed keywords

1 (4 ACETYLPIPERAZIN 1 YL) 4 PROPOXY 9H THIOXANTHEN 9 ONE; 1 [2 (1H BENZIMIDAZOL 2 YL)ETHANAMINE] 4 PROPOXY 9H THIOXANTHEN 9 ONE; 1 [[2 (4 NITROPHENYL)ETHYL]AMINO] 4 PROPOXY 9H THIOXANTHEN 9 ONE; 1 [[2 (DIETHYLAMINO)ETHYL]AMINO] 4 PROPOXY 9H THIOXANTHEN 9 ONE; DOXORUBICIN; GLYCOPROTEIN P; MIBEFRADIL; QUINIDINE; RHODAMINE 123; THIOXANTHENE DERIVATIVE; UNCLASSIFIED DRUG; VERAPAMIL;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL STRAIN K 562; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CROSS COUPLING REACTION; DRUG SYNTHESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR DOCKING; PRIORITY JOURNAL; TUMOR GROWTH;

ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; GROWTH INHIBITORS; HUMANS; K562 CELLS; P-GLYCOPROTEIN; THIOXANTHENES; XANTHONES;

EID: 81855198003     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.10.004     Document Type: Article

References (71)

1. C.F. Higgins Multiple molecular mechanisms for multidrug resistance transporters Nature 446 2007 749 757
2. E. Teodori, S. Dei, S. Scapecchi, and F. Gualtieri The medicinal chemistry of multidrug resistance (MDR) reversing drugs Farmaco 57 2002 385 415
3. C.F. Higgins The multidrug resistance P-glycoprotein Curr Opin Cell Biol 5 1993 684 687
4. H. Lage MDR1/P-glycoprotein (ABCB1) as target for RNA interference-mediated reversal of multidrug resistance Curr Drug Targets 7 2006 813 821
5. R. Clarke, F. Leonessa, and B. Trock Multidrug resistance/P-glycoprotein and breast cancer: review and meta-analysis Semin Oncol 32 2005 S9 S15
6. B.C. Baguley Novel strategies for overcoming multidrug resistance in cancer BioDrugs 16 2002 97 103
7. K. Takara, T. Sakaeda, and K. Okumura An update on overcoming MDR1-mediated multidrug resistance in cancer chemotherapy Curr Pharm Des 12 2006 273 286
8. R. Morphy, C. Kay, and Z. Rankovic From magic bullets to designed multiple ligands Drug Discov Today 9 2004 641 651
9. R. Morphy, and Z. Rankovic Designing multiple ligands-medicinal chemistry strategies and challenges Curr Pharm Des 15 2009 587 600
10. P. Zhan, and X. Liu Designed multiple ligands: an emerging anti-HIV drug discovery paradigm Curr Pharm Des 15 2009 1893 1917
11. A. Cavalli, M.L. Bolognesi, A. Minarini, M. Rosini, V. Tumiatti, and M. Recanatini Multi-target-directed ligands to combat neurodegenerative diseases J Med Chem 51 2008 347 372
12. M.B. Youdim, and J.J. Buccafusco Multi-functional drugs for various CNS targets in the treatment of neurodegenerative disorders Trends Pharmacol Sci 26 2005 27 35
13. C. Hu, D. Xu, W. Du, S. Qian, L. Wang, and J. Lou Novel 4 beta-anilino-podophyllotoxin derivatives: design synthesis and biological evaluation as potent DNA-topoisomerase II poisons and anti-MDR agents Mol Biosyst 6 2010 410 420
14. T.H. Corbett, C. Panchapor, L. Polin, N. Lowichik, S. Pugh, and K. White Preclinical efficacy of thioxanthone SR 271425 against transplanted solid tumors of mouse and human origin Invest New Drugs 17 1999 17 27
15. J.P. Stevenson, D. DeMaria, D. Reilly, J.D. Purvis, M.A. Graham, and G. Lockwood Phase I/pharmacokinetic trial of the novel thioxanthone SR 233377 (WIN33377) on a 5-day schedule Cancer Chemother Pharmacol 44 1999 228 234
16. D.N. Tchamo, M.G. Dijoux-Franca, A.M. Mariotte, E. Tsamo, J.B. Daskiewicz, and C. Bayet Prenylated xanthones as potential P-glycoprotein modulators Bioorg Med Chem Lett 10 2000 1343 1345
17. L. Pica-Mattoccia, and D. Cioli Studies on the mode of action of oxamniquine and related schistosomicidal drugs Am J Trop Med Hyg 34 1985 112 118
18. D. Rosi, G. Peruzzotti, E.W. Dennis, D.A. Berberian, H. Freele, and B.F. Tullar Hycanthone, a new active metabolite of lucanthone J Med Chem 10 1967 867 876
19. D. Cioli, L. Pica-Mattoccia, and S. Archer Antischistosomal drugs: past, present and future? Pharmacol Ther 68 1995 35 85
20. P.E. Hartman, P.B. Hulbert, E. Bueding, and D.D. Taylor Microsomal activation to mutagens of antischistosomal methyl thioxanthenones and initial tests on a possibly non-mutagenic analogue Mutat Res 31 1975 87 95
21. P.M. LoRusso, B.J. Foster, A. Wozniak, L.K. Heilbrun, J.I. McCormick, and P.E. Ruble Phase I pharmacokinetic study of the novel antitumor agent SR 233377 Clin Cancer Res 6 2000 3088 3094
22. M. Campone, N. Isambert, E. Bourbouloux, S. Maury, P. Monin-Baroille, and J. Berille Phase I dose-escalation study of a novel antitumor agent, SR 271425, administered intravenously in split doses (d1-d2-d3) in patients with refractory solid tumors Cancer Chemother Pharmacol 59 2007 689 695
23. P.H. Goncalves, F. High, P. Juniewicz, G. Shackleton, J. Li, and S. Boerner Phase I dose-escalation study of the thioxanthone SR 271425 administered intravenously once every 3 weeks in patients with advanced malignancies Invest New Drugs 26 2008 347 354
24. R. Anton, S. Barlow, and F. Toldrá Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the commission related to 2-isopropyl thioxanthone (ITX) and 2-ethylhexyl-4-dimethylaminobenzoate (EHDAB) in food contact materials EFSA J 293 2005 1 15
25. 1-Chloro-4-propoxy-9H-thioxanthen-9-one safety datasheet 2010 S-AC Ltd.
26. C.A. McDevitt, and R. Callaghan How can we best use structural information on P-glycoprotein to design inhibitors? Pharmacol Ther 113 2007 429 441
27. K.F. Chan, Y. Zhao, B.A. Burkett, I.L. Wong, L.M. Chow, and T.H. Chan Flavonoid dimers as bivalent modulators for P-glycoprotein-based multidrug resistance: synthetic apigenin homodimers linked with defined-length poly(ethylene glycol) spacers increase drug retention and enhance chemosensitivity in resistant cancer cells J Med Chem 49 2006 6742 6759
28. Z. Zsoldos, D. Reid, A. Simon, B.S. Sadjad, and A.P. Johnson eHiTS: an innovative approach to the docking and scoring function problems Curr Protein Pept Sci 7 2006 421 435
29. Z. Zsoldos, D. Reid, A. Simon, S.B. Sadjad, and A.P. Johnson eHiTS: a new fast, exhaustive flexible ligand docking system J Mol Graph Model 26 2007 198 212
30. N.M. O'Boyle, C. Morley, and G.R. Hutchison Pybel: a Python wrapper for the OpenBabel cheminformatics toolkit Chem Cent J 2 2008 5
31. R. Ordog PyDeT, a PyMOL plug-in for visualizing geometric concepts around proteins Bioinformation 2 2008 346 347
32. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, and E.C. Meng UCSF Chimera-a visualization system for exploratory research and analysis J Comput Chem 25 2004 1605 1612
33. A. Palmeira, F. Rodrigues, E. Sousa, M. Pinto, M. Helena Vasconcelos, and M.X. Fernandes New uses for old drugs: pharmacophore-based screening for the discovery of P-glycoprotein inhibitors Chem Biol Drug Des 78 1 2011 57 72
34. Promega. Technical Bulletin-Pgp-Glo™ Assay Systems. https://promega.es/tbs/tb341/tb341.pdf.
35. R.B. Wang, C.L. Kuo, L.L. Lien, and E.J. Lien Structure-activity relationship: analyses of p-glycoprotein substrates and inhibitors J Clin Pharm Ther 28 2003 203 228
36. I. Kostakis, K. Ghirtis, N. Pouli, P. Marakos, A.L. Skaltsounis, and S. Leonce Synthesis and cytotoxic activity of 2-dialkylaminoethylamino substituted xanthenone and thioxanthenone derivatives Farmaco 55 2000 455 460
37. G. Kolokythas, I.K. Kostakis, N. Pouli, P. Marakos, D. Kletsas, and H. Pratsinis Synthesis and cytotoxic activity of some new azapyranoxanthenone aminoderivatives Bioorg Med Chem 11 2003 4591 4598
38. G. Kolokythas, I.K. Kostakis, N. Pouli, P. Marakos, A.L. Skaltsounis, and H. Pratsinis Design and synthesis of some new pyranoxanthenone aminoderivatives with cytotoxic activity Bioorg Med Chem Lett 12 2002 1443 1446
39. A.A. Patchett, and R.P. Nargund Privileged structures-an update Annual reports in medicinal chemistry 2000 Academic Press p. 289-298, Chapter 26
40. R.W. DeSimone, K.S. Currie, S.A. Mitchell, J.W. Darrow, and D.A. Pippin Privileged structures: applications in drug discovery Comb Chem High Throughput Screen 7 2004 473 494
41. A.T. Serajuddin Salt formation to improve drug solubility Adv Drug Deliv Rev 59 2007 603 616
42. C.A. Lipinski Chris Lipinski discusses life and chemistry after the Rule of Five Drug Discov Today 8 2003 12 16
43. F. Lang, D. Zewge, I.N. Houpis, and R.P. Volante Amination of aryl halides using copper catalysis Tetrahedron Lett 42 2001 3251 3254
44. G. Consiglio, V. Frenna, E. Mezzina, A. Pizzolato, and A. Spinelli Catalysis in aromatic nucleophilic substitution, Part 12. Kinetics of the reactions of some 2-phenoxy-and 2-(p-nitrophenoxy)-3-nitro-5-X-thiophenes with benzylamine and N-benzylmethylamine in benzene J Chem Soc Perkin Trans 2 1998 325 333
45. T. Emokpae, P. Uwakwe, and J. Hirst The effect of ortho substituents on the mechanism of aromatic nucleophilic substitution reactions in dipolar aprotic solvents J Chem Soc Perkin Trans 2 1993 125 132
46. C. Tao, J. Li, Y. Fu, L. Liua, and Q. Guo Copper-catalyzed synthesis of primary arylamines from aryl halides and 2,2,2-trifluoroacetamide Tetrahedron Lett 49 2008 70 75
47. S. Caddick, and R. Fitzmaurice Microwave enhanced synthesis Tetrahedron 65 2009 3325 3355
48. M. Kidwai, P. Sapra, and B. Dave A facile method for nucleophilic aromatic substitution of cyclic amine Synth Commun 30 2000 4479 4488
49. G. Salmoria, E. Dall'Oglio, and C. Zucco Aromatic nucleophilic substitutions under microwave irradiation Tetrahedron Lett 39 1998 2471 2474
50. D. Prim, and G. Kirsch Convenient amination of weakly activated thiophenes, furans and selenophenes in aqueous media Tetrahedron 55 1999 6511 6526
51. Y. Cherng Efficient nucleophilic substitution reaction of aryl halides with amino acids under focused microwave irradiation Tetrahedron 56 2000 8287 8289
52. S. Weissman, and D. Zewge Recent advances in ether dealkylation Tetrahedron 61 2005 7833 7863
53. C.A. Tatu, V. Paunescu, D.I. Stanescu, and F. Schneider P-glycoprotein mediated multidrug resistance assessment by flow-cytometry in malignant hemopathies Anticancer Res 17 1997 2583 2586
54. E.J. Wang, C.N. Casciano, R.P. Clement, and W.W. Johnson In vitro flow cytometry method to quantitatively assess inhibitors of P-glycoprotein Drug Metab Dispos 28 2000 522 528
55. Y. Akazawa, H. Kawaguchi, M. Funahashi, Y. Watanabe, K. Yamaoka, and M. Hashida Effect of interferons on P-glycoprotein-mediated rhodamine-123 efflux in cultured rat hepatocytes J Pharm Sci 91 2002 2110 2115
56. C. Coburger, J. Wollmann, C. Baumert, M. Krug, J. Molnar, and H. Lage Novel insight in structure-activity relationship and bioanalysis of P-glycoprotein targeting highly potent tetrakishydroxymethyl substituted 3,9-diazatetraasteranes J Med Chem 51 2008 5871 5874
57. C. Ludescher, J. Thaler, D. Drach, J. Drach, M. Spitaler, and C. Gattringer Detection of activity of P-glycoprotein in human tumour samples using rhodamine 123 Br J Haematol 82 1992 161 168
58. J. Petriz, J.E. O'Connor, M. Carmona, and J. Garcia-Lopez Is rhodamine 123 an appropriate fluorescent probe to assess P-glycoprotein mediated multidrug resistance in vinblastine-resistant CHO cells? Anal Cell Pathol 14 1997 129 140
59. M. Denis-Gay, J.M. Petit, and M.H. Ratinaud Rhodamine 123: is it an appropriate dye to study P-glycoprotein activity in adriamycin-resistant K562 cells? Anticancer Res 15 1995 121 126
60. C.A. Slapak, N. Mizunuma, and D.W. Kufe Expression of the multidrug resistance associated protein and P-glycoprotein in doxorubicin-selected human myeloid leukemia cells Blood 84 1994 3113 3121
61. R.B. Kim Drugs as P-glycoprotein substrates, inhibitors, and inducers Drug Metab Rev 34 2002 47 54
62. M. Garrigos, L.M. Mir, and S. Orlowski Competitive and non-competitive inhibition of the multidrug-resistance-associated P-glycoprotein ATPase-further experimental evidence for a multisite model Eur J Biochem 244 1997 664 673
63. T. Litman, T. Zeuthen, T. Skovsgaard, and W.D. Stein Competitive, non-competitive and cooperative interactions between substrates of P-glycoprotein as measured by its ATPase activity Biochim Biophys Acta 1361 1997 169 176
64. S. Belli, P.M. Elsener, H. Wunderli-Allenspach, and S.D. Kramer Cholesterol-mediated activation of P-glycoprotein: distinct effects on basal and drug-induced ATPase activities J Pharm Sci 98 2009 1905 1918
65. I.L. Urbatsch, M.K. al-Shawi, and A.E. Senior Characterization of the ATPase activity of purified Chinese hamster P-glycoprotein Biochemistry 33 1994 7069 7076
66. G. Dayan, J.M. Jault, H. Baubichon-Cortay, L.G. Baggetto, J.M. Renoir, and E.E. Baulieu Binding of steroid modulators to recombinant cytosolic domain from mouse P-glycoprotein in close proximity to the ATP site Biochemistry 36 1997 15208 15215
67. N. Maki, P. Hafkemeyer, and S. Dey Allosteric modulation of human P-glycoprotein. Inhibition of transport by preventing substrate translocation and dissociation J Biol Chem 278 2003 18132 18139
68. C. Martin, G. Berridge, C.F. Higgins, and R. Callaghan The multi-drug resistance reversal agent SR 33557 and modulation of vinca alkaloid binding to P-glycoprotein by an allosteric interaction Br J Pharmacol 122 1997 765 771
69. G.D. Eytan, R. Regev, G. Oren, and Y.G. Assaraf The role of passive transbilayer drug movement in multidrug resistance and its modulation J Biol Chem 271 1996 12897 12902
70. Dongping M. Identify P-glycoprotein substrates and inhibitors with the rapid, HTS Pgp-Glo™ assay system. Promega Notes; 2007.
71. C. Bailly, and M.J. Waring Preferential intercalation at AT sequences in DNA by lucanthone, hycanthone, and indazole analogs. A footprinting study Biochemistry 32 1993 5985 5993