Flavonoid structure-activity studies identify 6-prenylchrysin and tectochrysin as potent and specific inhibitors of breast cancer resistance protein ABCG2

Cancer Research

Volumn 65, Issue 11, 2005, Pages 4852-4860

  Ahmed Belkacem, Abdelhakim ^a   Pozza, Alexandre ^a   Muñoz Martínez, Francisco ^b   Bates, Susan E ^c   Castanys, Santiago ^b   Gamarro, Francisco ^b   Pietro, Attilio Di ^a   Pérez Victoria, José M ^a,b  

^a INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^b INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 PRENYLCHRYSIN; BREAST CANCER RESISTANCE PROTEIN; ELACRIDAR; FLAVANONE; FLAVONE; FLAVONOID; FLAVONOL; GLYCOPROTEIN P; ISOFLAVONE; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; TECTOCHRYSIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL GROWTH; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; DRUG INTERACTION; DRUG POTENCY; DRUG SENSITIVITY; DRUG TRANSPORT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PRENYLATION; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ACRIDINES; ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; BENZIMIDAZOLES; CELL LINE; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FLAVONOIDS; HUMANS; MITOXANTRONE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; RHODAMINES; STRUCTURE-ACTIVITY RELATIONSHIP; TETRAHYDROISOQUINOLINES; TRANSFECTION;

EID: 19644378841     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-1817     Document Type: Article

References (46)

1. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976;455:152-62.
2. Cole SP, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992;258:1650-4,
3. Allikmets R, Schriml LM, Hutchinson A, Romano-Spica V, Dean M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 1998;58:5337-9.
4. Doyle LA, Yang W, Abruzzo LV, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci U S A 1998;95:15665-70.
5. Miyake K, Mickley L, Litman T, et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 1999;59:8-13.
6. Ozvegy C, Litman T, Szakacs G, et al. Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem Biophys Res Commun 2001;285:111-7.
7. Xu J, Yang Y. Bates S, Zhang JT. Characterization of oligomeric human half-transporter ATP-binding cassette G2. J Biol Chem 2004;279:19781-9.
8. Doyle LA, Ross DD. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 2003;22:7340-58.
9. Sarkadi B, Ozvegy-Laczka C, Nemet K, Varadi A. ABCG2: a transporter for all seasons. FEBS Lett 2004;567:116-20.
10. Honjo Y, Morísaki K, Huff LM, et al. Single-nucleotide polymorphism (SNP) analysis in the ABC half-transporter ABCG2 (MXR/BCRP/ABCP1). Cancer Biol Ther 2002;1:696-702.
11. Bates SE, Robey R, Miyake K, Rao K, Ross DD, Litman T. The role of half-transporters in multidrug resistance. J Bioenerg Biomembr 2001;33:503-11.
12. Castro AF, Altenberg GA. Inhibition of drug transport by genistein in multidrug-resistant cells expressing P-glycoprotein. Biochem Pharmacol 1997;53:89-93.
13. Shapiro AB, Ling V, Effect of quercetin on Hoechst33342 transport by purified and reconstituted P-glycoprotein, Biochem Pharmacol 1997;53:587-96.
14. Conseil G, Baubichon-Cortay H, Dayan G, Jault JM, Barron D, Di Pietro A. Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc Natl Acad Sci U S A 1998;95:9831-6.
15. Di Pietro A, Conseil G, Perez-Victoria JM, et al. Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell Mol Life Sci 2002;59:307-22.
16. Hooijberg JH, Broxterman HJ, Heijn M, Fles DLA, Lankelma J, Pinedo HM. Modulation by (iso)flavonoids of the ATPase activity of the multidrug resistance protein. FEBS Lett 1997;413:344-8.
17. Leslie EM, Mao Q, Oleschuk CJ, Deeley RG, Cole SPC. Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol Pharmacol 2001;59:1171-80.
18. Trompier D, Baubichon-Cortay H, Chang XB, et al. Multiple flavonoid-binding sites within multidrug resistance protein MRP1. Cell Mol Life Sci 2003;60:2164-77.
19. Perez-Victoria JM, Chiquero MJ, Conseil G, et al. Correlation between the affinity of flavonoids binding to the cytosolic site of Leishmania tropica multidrug transporter and their efficiency to revert parasite resistance to daunomycin. Biochemistry 1999;38:1736-43.
20. Perez-Victoria JM, Di Pietro A, Barron D, Ravelo AG, Castanys S, Gamarro F. Multidrug resistance phenotype mediated by the P-glycoprotein-like transporter in Leishmania: a search for reversal agents. Curr Drug Targets 2002;3:311-33.
21. Conseil G, Decottignies A, Jault JM, et al. Prenyl-flavonoids as potent inhibitors of the Pdr5p multidrug ABC transporter from Saccharomyces cerevisiae. Biochemistry 2000;39:6910-7.
22. Middleton E Jr, Kandaswami C, Theoharides TC. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol Rev 2000;52:673-751.
23. Robey RW, Medina-Perez WY, Nishiyama K, et al. Overexpression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells. Clin Cancer Res 2001;7:145-52.
24. Perez-Victoria JM, Pozza A, Ahmed-Belkacem A, Lazzaroni J-C, Di Pietro A. High Overexpression of human breast cancer resistance protein in the plasma membrane of a mutant Escherichia coli and selection of flavonoid inhibitors. 4th FEBS Advanced Lecture Course "ATP-binding cassette (ABC) proteins: from genetic disease to multidrug resistance," March 1-8, 2003, Gosau (Austria).
25. Cooray HC, Janvilisri T, van Veen HW, Hladky SB, Barrand MA. Interaction of the breast cancer resistance protein with plant polyphenols. Biochem Biophys Res Commun 2004;317:269-75.
26. Zhang S, Yang X, Morris ME. Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Mol Pharmacol 2004;65:1208-16.
27. Imai Y, Tsukahara S, Asada S. Sugimoto Y. Phytoestrogen/flavanoids reverse breast cancer resistance protein/ABCG2-mediated multidrug resistance. Cancer Res 2004;64:4346-52.
28. Comte G. Daskiewicz JB, Bayet C, et al. C-Isoprenylation of flavonoids enhances binding affinity toward P-glycoprotein and modulation of cancer cell chemoresistance. J Med Chem 2001;44:763-8.
29. Robey RW, Honjo Y, Morisaki K, et al. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 2003;89:1971-8.
30. Cardarelli CO, Aksentijevich I, Pastan I, Gottesman MM. Differential effects of P-glycoprotein inhibitors on NIH3T3 cells transfected with wild-type (G185) or mutant (V185) multidrug transporters. Cancer Res 1995;55:1086-91.
31. Kool M, van der Linden M, de Haas M, et al. MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci U S A 1999;96:6914-9.
32. Sarver JG, Klis WA, Byers JP, Erhardt PW. Microplate screening of the differential effects of test agents on Hoechst 33342, rhodamine 123, and rhodamine 6G accumulation in breast cancer cells that overexpress P-glycoprotein. J Biomol Screen 2002;7:29-34.
33. Dey S, Ramachandra M, Pastan I, Gottesman MM, Ambudkar SV. Photoaffinity labeling of human P-glycoprotein: effect of modulator interaction and ATP hydrolysis on substrate binding. Methods Enzymol 1998;292:318-28.
34. Van Veldhoven PP, Mannaerts GP. Inorganic and organic phosphate measurements in the nanomolar range. Anal Biochem 1987;161:45-8.
35. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
36. Woehlecke H, Osada H, Herrmann A, Lage H. Reversal of breast cancer resistance protein-mediated drug resistance by tryprostatin A. Int J Cancer 2003;107:721-8.
37. Perez-Victoria FJ, Conseil G, Munoz-Martinez F, et al. RU49953: a non-hormonal steroid derivative that potently inhibits P-glycoprotein and reverts cellular multidrug resistance. Cell Mol Life Sci 2003;60:526-35.
38. Robey RW, Honjo Y, van de Laar A, et al. A functional assay for detection of the mitoxantrone resistance protein. MXR (ABCG2). Biochim Biophys Acta 2001;1512:171-82.
39. Ozvegy-Laczka C, Koblos G, Sarkadi B, Varadi A. Single amino acid (482) variants of the ABCG2 multidrug transporter: major differences in transport capacity and substrate recognition. Biochim Biophys Acta 2005;1668:53-63.
40. Schumacher MA, Miller MC, Brennan RG. Structural mechanism of the simultaneous binding of two drugs to a multidrug-binding protein. EMBO J 2004;23:2923-30.
41. Robey RW, Steadman K, Polgar O, et al. Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res 2004;64:1242-6.
42. Kerr KM, Sauna ZE, Ambudkar SV. Correlation between steady-state ATP hydrolysis and vanadate-induced ADP trapping in Human P-glycoprotein. Evidence for ADP release as the rate-limiting step in the catalytic cycle and its modulation by substrates. J Biol Chem 2001;276:8657-64.
43. Chang XB, Hou YX, Riordan JR. Stimulation of ATPase activity of purified multidrug resistance-associated protein by nucleoside diphosphates. J Biol Chem 1998;273:23844-8.
44. Nakanishi T, Doyle LA, Hassel B, et al. Functional characterization of human breast cancer resistance protein (BCRP, ABCG2) expressed in the oocytes of Xenopus laevis. Mol Pharmacol 2003;64:1452-62.
45. de Bruin M, Miyake K, Litman T, Robey R, Bates SE. Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR. Cancer Lett 1999;146:117-26.
46. Allen JD, van Loevezijn A, Lakhai JM, et al. Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 2002;1:417-25.