Quercetin: A potential drug to reverse multidrug resistance

Life Sciences

Volumn 87, Issue 11-12, 2010, Pages 333-338

  Chen, Chen ^a   Zhou, Jane ^b   Ji, Chunyan ^a  

^a SHANDONG UNIVERSITY   (China)

^b Zenith Diagnostic Consultants   (United States)

Author keywords

Breast cancer resistance protein; Multidrug resistance; Multidrug resistance associated protein; P glycoprotein; Quercetin

Indexed keywords

5 ACETAMIDOSALICYLIC ACID; BREAST CANCER RESISTANCE PROTEIN; CIMETIDINE; CISPLATIN; DAUNORUBICIN; DIGOXIN; DILTIAZEM; DOXORUBICIN; ETOPOSIDE; FEXOFENADINE; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; PRAZOSIN; QUERCETIN; RHODAMINE 123; TAMOXIFEN; TOPOTECAN; VINBLASTINE; ABC TRANSPORTER;

CANCER RESISTANCE; CHEMOSENSITIZATION; DRUG ACTIVITY; DRUG MECHANISM; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MULTIDRUG RESISTANCE; NONHUMAN; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; NEOPLASMS;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, MULTIPLE; HUMANS; NEOPLASMS; QUERCETIN;

EID: 77956414625     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2010.07.004     Document Type: Review

References (92)

1. Abrahamse S.L., Kloots W.J., van Amelsvoort J.M.M. Absorption, distribution, and secretion of epicatechin and quercetin in the rat. Nutrition Research 2005, 25(3):305-317.
2. Ader P., Wessmann A., Wolffram S. Bioavailability and metabolism of the flavonol quercetin in the pig. Free Radical Biology & Medicine 2000, 28(7):1056-1067.
3. Akbas S.H., Timur M., Ozben T. The effect of quercetin on topotecan cytotoxicity in MCF-7 and MDA-MB 231 human breast cancer cells. The Journal of Surgical Research 2005, 125(1):49-55.
4. Ambudkar S.V., Kimchi-Sarfaty C., Sauna Z.E., Gottesman M.M. P-glycoprotein: from genomics to mechanism. Oncogene 2003, 22(47):7468-7485.
5. Bansal T., Awasthi A., Jaggi M., Khar R.K., Talegaonkar S. Pre-clinical evidence for altered absorption and biliary excretion of irinotecan (CPT-11) in combination with quercetin: possible contribution of P-glycoprotein. Life Sciences 2008, 83(7-8):250-259.
6. Bokkenheuser V.D., Shackleton C.H.L., Winter J. Hydrolysis of dietary flavonoid glycosides by strains of intestinal Bacteroides from human. The Biochemical Journal 1987, 248(3):953-956.
7. Bors W., Heller W., Michel C., Saran M. Flavonoids as antioxidants: determination of radical scavenging efficiencies. Methods in Enzymology 1990, 186:343-355.
8. Chang X.B. A molecular understanding of ATP-dependent solute transport by multidrug resistance-associated protein MRP1. Cancer and Metastasis Reviews 2007, 26(1):15-37.
9. Chen X., Yin O.Q., Zuo Z., Chow M.S. Pharmacokinetics and modeling of quercetin and metabolites. Pharmaceutical Research 2005, 22(6):892-901.
10. Chen W., Wang X., Zhuang J., Zhang L., Lin Y. Induction of death receptor 5 and suppression of survivin contribute to sensitization of TRAIL-induced cytotoxicity by quercetin in non-small cell lung cancer cells. Carcinogenesis 2007, 28(10):2114-2121.
11. Chieli E., Romiti N., Rodeiro I., et al. In vitro effects of Mangifera indica and polyphenols derived on ABCB1/P-glycoprotein activity. Food and Chemical Toxicology 2009, 47(11):2703-2710.
12. Choi J.S., Jo B.W., Kim Y.C. Enhanced paclitaxel bioavailability after oral administration of paclitaxel or prodrug to rats pretreated with quercetin. European Journal of Pharmaceutics and Biopharmaceutics 2004, 57(2):313-318.
13. Chung S.Y., Sung M.K., Kim N.H., Jang J.O., Go E.J., Lee H.J. Inhibition of P-glycoprotein by natural products in human breast cancer cells. Archives of Pharmacal Research 2005, 28(7):823-828.
14. Cole S.P., Deeley R.G. Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays 1998, 20(11):931-940.
15. Cole S.P., Deeley R.G. Transport of glutathione and glutathione conjugates by MRP1. Trends in Pharmacological Sciences 2006, 27(8):438-446.
16. Conseil G., Baubichon-Cortay H., Dayan G., Jault J.M., Barron D., Di Pietro A. Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(17):9831-9836.
17. Cooray H.C., Janvilisri T., van Veen H.W., Hladky S.B., Barrand M.A. Interaction of the breast cancer resistance protein with plant polyphenols. Biochemical and Biophysical Research Communications 2004, 317(1):269-275.
18. Cornard J.P., Dangleterre L., Lapouge C. Computational and spectroscopic characterization of the molecular and electronic structure of the Pb(II)-quercetin complex. The Journal of Physical Chemistry 2005, 109(44):10044-10051.
19. Critchfield J.W., Welsh C.J., Phang J.M., Yeh G.C. Modulation of adriamycin accumulation and efflux by flavonoids in HCT-15 colon cells. Activation of P-glycoprotein as a putative mechanism. Biochemical Pharmacology 1994, 48(7):1437-1445.
20. Day A.J., Diaz J.C., Kroon P.A., McLauchlan R., Faulds C.B., Plumb G.W., et al. Dietary flavonoid and isoflavone glycosides are hydrolysed by the lactase site of lactase phlorizin hydrolase. FEBS Letters 2000, 468:166-170.
21. de Boer V.C., Dihal A.A., van der Woude H., Arts I.C., Wolffram S., Alink G.M., Rietjens I.M., Keijer J., Hollman P.C. Tissue distribution of quercetin in rats and pigs. The Journal of Nutrition 2005, 135(7):1718-1725.
22. De Vincenzo R., Ferlini C., Distefano M., Gaggini C., Riva A., Bombardelli E., et al. In vitro evaluation of newly developed chalcone analogues in human cancer cells. Cancer Chemotherapy and Pharmacology 2000, 46(4):305-312.
23. Doyle L.A., Yang W., Abruzzo L.V., Krogmann T., Gao Y., Rishi A.K., Ross D.D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(26):15665-15670.
24. Duraj J., Zazrivcova K., Bodo J., et al. Flavonoid quercetin, but not apigenin or luteolin, induced apoptosis in human myeloid leukemia cells and their resistant variants. Neoplasma 2005, 52(4):273-279.
25. Ebert B., Seidel A., Lampen A. Phytochemicals induce breast cancer resistance protein in Caco-2 cells and enhance the transport of benzo[a]pyrene-3-sulfate. Toxicological Sciences 2007, 96(2):227-236.
26. Efferth T., Davey M., Olbrich A., Rücker G., Gebhart E., Davey R. Activity of drugs from traditional Chinese medicine toward sensitive and MDR1- or MRP1-overexpressing multidrug-resistant human CCRF-CEM leukemia cells. Blood Cells, Molecules & Diseases 2002, 28(2):160-168.
27. Ejendal K.F., Hrycyna C.A. Multidrug resistance and cancer: the role of the human ABC transporter ABCG2. Current Protein & Peptide Science 2002, 3(5):503-511.
28. Erlund I. Review of the flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, and epidemiology. Nutrition Research 2004, 24(10):851-874.
29. Ferry D.R., Smith A., Malkhandi J., Fyfe D.W., de Takats P.G., Anderson D., Baker J., Kerr D.J. Phase I clinical trial of the flavonoid quercetin: pharmacokinetics and evidence for in vivo tyrosine kinase inhibition. Clinical Cancer Research 1996, 2(4):659-668.
30. Fukuda I., Ashida H. Suppressive effects of flavonoids on activation of the aryl hydrocarbon receptor induced by dioxins. Functional Foods and Health, ACS Symposium Series 2008, 368-374. American Chemical Society, Washington DC. T. Shibamoto, F. Shahidi, K. Kanazawa, C.T. Ho (Eds.).
31. Granado-Serrano A.B., Martin M.A., Bravo L., Goya L., Ramos S. Quercetin induces apoptosis via caspase activation, regulation of Bcl-2, and inhibition of PI-3-kinase/Akt and ERK pathways in a human hepatoma cell line (HepG2). The Journal of Nutrition 2006, 136(11):2715-2721.
32. Hertog M.G., Feskens E.J., Hollman P.C., Katan M.B., Kromhout D. Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly study. Lancet 1993, 342(8878):1007-1011.
33. Hertog M.G., Kromhout D., Aravanis C., Blackburn H., Buzina R., Fidanza F., et al. Flavonoid intake and long-term risk of coronary heart disease and cancer in the seven countries study. Archives of Internal Medicine 1995, 155(4):381-386.
34. Hipfner D.R., Almquist K.C., Leslie E.M., Gerlach J.H., Grant C.E., Deeley R.G., Cole S.P. Membrane topology of the multidrug resistance protein (MRP). A study of glycosylation-site mutants reveals an extracytosolic NH2 terminus. The Journal of Biological Chemistry 1997, 272(38):23623-23630.
35. Hollman P.C., Katan M.B. Absorption, metabolism and health effects of dietary flavonoids in man. Biomedicine & Pharmacotherapy 1997, 51(8):305-310.
36. Ikegawa T., Ohtani H., Koyabu N., Juichi M., Iwase Y., Ito C., et al. Inhibition of P-glycoprotein by flavonoid derivatives in adriamycin-resistant human myelogenous leukemia (K562/ADM) cells. Cancer Letters 2002, 177(1):89-93.
37. Jakubowicz-Gil J., Paduch R., Piersiak T., Glowniak K., Gawron A., Kandefer-Szersze? M. The effect of quercetin on pro-apoptotic activity of cisplatin in HeLa cells. Biochemical Pharmacology 2005, 69(9):1343-1350.
38. Jakubowicz-Gil J., Rzeski W., Zdzisinska B., et al. Different sensitivity of neurons and neuroblastoma cells to quercetin treatment. Acta Neurobiologiae Eexperimentalis 2008, 68(4):463-476.
39. Jing S., Zhang W.J., Wu J., Zhu Y.F. The synergistic reversal effect of multidrug resistance by quercetin and hyperthermia in doxorubicin-resistant human myelogenous leukemia cells. International Journal of Hyperthermia 2008, 24(2):151-159.
40. Kim S.H., Yeo A.S., Lim Y.S., Kang C.D., Kim C.M., Chung B.S. Suppression of multidrug resistance via inhibition of heat shock factor by quercetin in MDR cells. Experimental & Molecular Medicine 1998, 30(2):87-92.
41. Kim W.K., Bang M.H., Kim E.S., Kang N.E., et al. Quercetin decreases the expression of ErbB2 and ErbB3 proteins in HT-29 human colon cancercells. The Journal of Nutritional Biochemistry 2005, 16(3):155-162.
42. Kim K.A., Park P.W., Park J.Y. Short-term effect of quercetin on the pharmacokinetics of fexofenadine, a substrate of P-glycoprotein, in healthy volunteers. European Journal of Clinical Pharmacology 2009, 65(6):609-614.
43. Kitagawa S., Nabekura T., Takahashi T., Nakamura Y., Sakamoto H., Tano H., Hirai M., Tsukahara G. Structureactivity relationships of the inhibitory effects of flavonoids on P-glycoprotein-mediated transport in KB-C2 cells. Biological & Pharmaceutical Bulletin 2005, 28(12):2274-2278.
44. Knekt P., Jarvinen R., Seppanen R., Hellovaara M., Teppo L., Pukkala E., Aromaa A. Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. American Journal of Epidemiology 1997, 146(3):223-230.
45. Kothan S., Dechsupa S., Leger G., Moretti J.L., Vergote J., Mankhetkorn S. Spontaneous mitochondrial membrane potential change during apoptotic induction by quercetin in K562 and K562/adr cells. Canadian Journal of Physiology and Pharmacology 2004, 82(12):1084-1090.
46. Krishna R., Mayer L.D. Multidrug resistance (MDR) in cancer-Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. European Journal of Pharmaceutical Sciences 2000, 11(4):265-283.
47. Lage H. An overview of cancer multidrug resistance: a still unsolved problem. Cellular and Molecular Life Sciences 2008, 65(20):3145-3167.
48. Leslie E.M., Mao Q., Oleschuk C.J., Deeley R.G., Cole S.P. Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Molecular Pharmacology 2001, 59(5):1171-1180.
49. Leslie E.M., Deeley R.G., Cole S.P. Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1(MRP1). Drug Metabolism and Disposition 2003, 31(1):11-15.
50. Li X.G., Choi J.S. Effects of quercetin on the pharmacokinetics of etoposide after oral or intravenous administration of etoposide in rats. Anticancer Research 2009, 29(4):1411-1415.
51. Lim J.C., Kania K.D., Wijesuriya H., Chawla S., Sethi J.K., Pulaski L., Romero I.A., Couraud P.O., et al. Activation of beta-catenin signalling by GSK-3 inhibition increases p-glycoprotein expression in brain endothelial cells. Journal of Neurochemistry 2008, 106(4):1855-1865.
52. Limtrakul P., Khantamat O., Pintha K. Inhibition of P-glycoprotein function and expression by kaempferol and quercetin. Journal of Chemotherapy 2005, 17(1):86-95.
53. Litman T., Druley T.E., Stein W.D., Bates S.E. From MDR to MXR: new understanding of multidrug resistance systems, their properties and clinical significance. Cellular and Molecular Life Sciences 2001, 58(7):931-959.
54. Liu Y., Liu Y., Dai Y., Xun L., Hu M. Enteric disposition and recycling of flavonoids and ginkgo flavonoids. Journal of Alternative and Complementary Medicine 2003, 9(5):631-640.
55. Loa J., Chow P., Zhang K. Studies of structure-activity relationship on plant polyphenol-induced suppression of human liver cancer cells. Cancer Chemotherapy and Pharmacology 2009, 63(6):1007-1016.
56. Loo T.W., Clarke D.M. Mutational analysis of ABC proteins. Archives of Biochemistry and Biophysics 2008, 476(1):51-64.
57. Manach C., Williamson G., Morand C., Scalbert A., Remesy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. The American Journal of Clinical Nutrition 2005, 81(1 Suppl):230-242.
58. Mendoza-Wilson Ana Maria, Glossman-Mitnik Daniel CHIH-DFT determination of the molecular structure, infrared and ultraviolet spectra of the flavonoid quercetin. Journal of Molecular Structure: THEOCHEM 2004, 681:71-76.
59. Mitsunaga Y., Takanaga H., Matsuo H., Naito M., Tsuruo T., Ohtani H., Sawada Y. Effect of bioflavonoids on vincristine transport across blood-brain barrier. European Journal of Pharmacology 2000, 395(3):193-201.
60. Moon Y.J., Wang X., Morris M.E. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicology in Vitro 2006, 20(2):187-210.
61. Moon Y.J., Wang L., DiCenzo R., Morris M.E. Quercetin pharmacokinetics in humans. Biopharmaceutics & Drug Disposition 2008, 29(4):205-217.
62. Murota K., Terao J. Antioxidative flavonoid quercetin: implication of its intestinal absorption and metabolism. Archives of Biochemistry and Biophysics 2003, 417(1):12-17.
63. Nemeth K., Plumb G.W., Berrin J.G., Juge N., Jacob R., Naim H.Y., et al. Deglycosylation by small intestinal epithelial cell beta-glucosidases is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans. European Journal of Nutrition 2003, 42(1):29-42.
64. Nguyen H., Zhang S.Z., Morris M.E. Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. Journal of Pharmaceutical Sciences 2003, 92(2):250-257.
65. Ohtani H., Ikegawa T., Honda Y., Kohyama N., Morimoto S., Shoyama Y., et al. Effects of various methoxyflavones on vincristine uptake and multidrug resistance to vincristine in P-gp-overexpressing K562/ADM Cells. Pharmaceutical Research 2007, 24(10):1936-1943.
66. Oliveira E.J., Watson D.G., Grant M.H. Metabolism of quercetin and kaempferol by rat hepatocytes and the identification of flavonoid glycosides in human plasma. Xenobiotica 2002, 32(4):279-287.
67. Psahoulia F.H., Drosopoulos K.G., Doubravska L., Andera L., Pintzas A. Quercetin enhances TRAIL-mediated apoptosis in colon cancer cells by inducing the accumulation of death receptors in lipid rafts. Molecular Cancer Therapeutics 2007, 6(9):2591-2599.
68. Ramos A.M., Aller P. Quercetin decreases intracellular GSH content and potentiates the apoptotic action of the antileukemic drug arsenic trioxide in human leukemia cell lines. Biochemical Pharmacology 2008, 75(10):1912-1923.
69. Rimm E.B., Katan M.B., Ascherio A., Stampfer M.J., Willett W.C. Relation between intake of flavonoids and risk for coronarty heart disease in male health professionals. Annals of Internal Medicine 1996, 125(5):384-389.
70. Scambia G., Ranelletti F.O., Panici P.B., De Vincenzo R., et al. Quercetin potentiates the effect of adriamycin in a multidrug-resistant MCF-7 human breast-cancer cell line: P-glycoprotein as a possible target. Cancer Chemotherapy and Pharmacology 1994, 34(6):459-464.
71. Shapiro A.B., Ling V. Extraction of Hoechst 33342 from the cytoplasmic leaflet of the plasma membrane by P-glycoprotein. European Journal of Biochemistry 1997, 250(1):122-129.
72. Shih H., Pickwell G.V., Quattrochi L.C. Differential effects of flavonoid compounds on tumor promoter-induced activation of the human CYP1A2 enhancer. Archives of Biochemistry and Biophysics 2000, 373(1):287-294.
73. Shin S.C., Choi J.S., Li X.G. Enhanced bioavailability of tamoxifen after oral administration of tamoxifen with quercetin in rats. International Journal of Pharmaceutics 2006, 313:144-149.
74. Siarheyeva A., Lopez J.J., Glaubitz C. Localization of multidrug transporter substrates within model membranes. Biochemistry 2006, 45(19):6203-6211.
75. Silva M.M., Santos M.R., Caroco G., Rocha R., Justino G., Mira L. Structure-antioxidant activity relationships of flavonoids: a re-examination. Free Radical Research 2002, 36(11):1219-1227.
76. Skupien K., Osmianski J., Kostrzewa-Nowak D., Tarasiuk J. In vitro antileukaemic activity of extracts from berry plant leaves against sensitive and multidrug resistant HL60 cells. Cancer Letters 2006, 236(2):282-291.
77. Skupien K., Kostrzewa-Nowak D., Oszmianski J., Tarasiuk J. In vitro antileukaemic activity of extracts from chokeberry (Aronia melanocarpa [Michx] Elliott) and mulberry (Morus alba L.) leaves against sensitive and multidrug resistant HL60 cells. Phytotherapy Research 2008, 22(5):689-694.
78. Taur J.S., Rodriguez-Proteau R. Effects of dietary flavonoids on the transport of cimetidine via P-glycoprotein and cationic transporters in Caco-2 and LLC-PK1 cell models. Xenobiotica 2008, 38(12):1536-1550.
79. Theoharides T.C., Bielory L. Mast cells and mast cell mediators as targets of dietary supplements. Annals of Allergy, Asthma & Immunology 2004, 93(2Suppl 1):S24-S34.
80. van Zanden J.J., Wortelboer H.M., Bijlsma S., Punt A., Usta M., Bladeren P.J., et al. Quantitative structure activity relationship studies on the flavonoid mediated inhibition of multidrug resistance proteins 1 and 2. Biochemical Pharmacology 2005, 69(4):699-708.
81. van Zanden J.J., van der Woude H., Vaessen J., et al. The effect of quercetin phase II metabolism on its MRP1 and MRP2 inhibiting potential. Biochemical Pharmacology 2007, 74(2):345-351.
82. Volate S.R., Davenport D.M., Muga S.J., Wargovich M.J. Modulation of aberrant crypt foci and apoptosis by dietary herbal supplements (quercetin, curcumin, silymarin, ginseng and rutin). Carcinogenesis 2005, 26(8):1450-1456.
83. Walle T., Walle U.K., Halushka P.V. Carbon dioxide is the major metabolite of quercetin in humans. The Journal of Nutrition 2001, 131(10):2648-2652.
84. Wang Y., Cao J., Zeng S. Establishment of a P-glycoprotein substrate screening model and its preliminary application. World Journal of Gastroenterology 2004, 10(9):1365-1368.
85. Wang Y.H., Chao P.D., Hsiu S.L., Wen K.C., Hou Y.C. Lethal quercetin-digoxin interaction in pigs. Life Sciences 2004, 74(10):1191-1197.
86. Williamson G., Baron D., Shimoi K., Terao J. In vitro biological properties of flavonoid conjugates found in vivo. Free Radical Research 2005, 39(5):457-469.
87. Wu C.P., Calcagno A.M., Hladky S.B., Ambudkar S.V., Barrand M.A. Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). The FEBS Journal 2005, 272(18):4725-4740.
88. Xing N., Chen Y., Mitchell S.H., Young C.Y. Quercetin inhibits expression and function of the androgen receptor in LNCaP prostate cancer cells. Carcinogenesis 2001, 22(3):409-414.
89. Yoshimura S., Kawano K., Matsumura R., et al. Inhibitory effect of flavonoids on the efflux of N-acetyl 5-aminosalicylic acid intracellularly formed in Caco-2 cells. Journal of Biomedicine & Biotechnology 2009, 467-489.
90. Zaman G.J., Lankelma J., van Tellingen O., Beijnen J., Dekker H., Paulusma C., et al. Role of glutathione in the export of compounds from cells by the multidrug-resistance -associated protein. Proceedings of the National Academy of Sciences of the United States of America 1995, 92(17):7690-7694.
91. Zhang K., Wong K.P. Inhibition of the efflux of glutathione S-conjugates by plant polyphenols. Biochemical Pharmacology 1996, 52(10):1631-1638.
92. Zhang S., Yang X.N., Morris M.E. Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Molecular Pharmacology 2004, 65(5):1208-1216.