In vitro effect of quercetin on human gastric carcinoma: Targeting cancer cells death and MDR

Food and Chemical Toxicology

Volumn 50, Issue 9, 2012, Pages 3375-3383

  Borska, Sylwia ^a   Chmielewska, Magdalena ^a   Wysocka, Teresa ^a   Drag Zalesinska, Malgorzata ^a   Zabel, Maciej ^a,b   Dziegiel, Piotr ^a,b,c  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

^c UNIVERSITY SCHOOL OF PHYSICAL EDUCATION   (Poland)

Author keywords

Apoptosis; Cytotoxcity; Drug resistance; Human gastric carcinoma cells; P glycoprotein; Quercetin

Indexed keywords

DAUNORUBICIN; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; QUERCETIN;

ABCB1 GENE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; DRUG TRANSPORT; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IC 50; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; INCUBATION TIME; MULTIDRUG RESISTANCE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STOMACH CARCINOMA; WESTERN BLOTTING;

APOPTOSIS; CELL LINE, TUMOR; DAUNORUBICIN; DRUG RESISTANCE, NEOPLASM; HUMANS; P-GLYCOPROTEIN; QUERCETIN; STOMACH NEOPLASMS;

EID: 84864360535     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.06.035     Document Type: Article

References (58)

1. Bakheet S.A. Assessment of anti-cytogenotoxic effects of quercetin in animals treated with topotecan. Oxid. Med. Cell Longev. 2011, 2011:824597.
2. Borska S., Gebarowska E., Wysocka T., Drag-Zalesinska M., Zabel M. Induction of apoptosis by EGCG in selected tumour cell lines in vitro. Folia Histochem. Cytobiol. 2003, 41:229-232.
3. Borska S., Gebarowska E., Wysocka T., Drag-Zalesinska M., Zabel M. The effects of quercetin vs cisplatin on proliferation and the apoptotic process in A549 and SW1271 cell lines in in vitro conditions. Folia Morphol. (Warsz) 2004, 63:103-105.
4. Borska S., Drag-Zalesinska M., Wysocka T., Sopel M., Dumanska M., Zabel M., Dziegiel P. Antiproliferative and pro-apoptotic effects of quercetin on human pancreatic carcinoma cell lines EPP85-181P and EPP85-181RDB. Folia Histochem. Cytobiol. 2010, 48:222-229.
5. Borska S., Sopel M., Chmielewska M., Zabel M., Dziegiel P. Quercetin as a potential modulator of P-glycoprotein expression and function in cells of human pancreatic carcinoma line resistant to daunorubicin. Molecules 2010, 15:857-870.
6. Bu T., Mi Y., Zeng W., Zhang C. Protective effect of quercetin on cadmium-induced oxidative toxicity on germ cells in male mice. Anat. Rec. (Hoboken) 2011, 294:520-526.
7. Cerda H., Delincee H., Haine H., Rupp H. The DNA 'comet assay' as a rapid screening technique to control irradiated food. Mutat. Res. 1997, 375:167-181.
8. Cheng S., Gao N., Zhang Z., Chen G., Budhraja A., Ke Z., Son Y.O., Wang X., Luo J., Shi X. Quercetin induces tumor-selective apoptosis through downregulation of Mcl-1 and activation of Bax. Clin. Cancer Res. 2010, 16:5679-5691.
9. Chieli E., Romiti N., Rodeiro I., Garrido G. In vitro modulation of ABCB1/P-glycoprotein expression by polyphenols from Mangifera indica. Chem. Biol. Interact. 2010, 186:287-294.
10. Choi Y.J., Jeong Y.J., Lee Y.J., Kwon H.M., Kang Y.H. (-)Epigallocatechin gallate and quercetin enhance survival signaling in response to oxidant-induced human endothelial apoptosis. J. Nutr. 2005, 135:707-713.
11. Choi J.S., Piao Y.J., Kang K.W. Effects of quercetin on the bioavailability of doxorubicin in rats: role of CYP3A4 and P-gp inhibition by quercetin. Arch. Pharm. Res. 2011, 34:607-613.
12. Colabufo N.A., Contino M., Berardi F., Perrone R., Panaro M.A., Cianciulli A., Mitolo V., Azzariti A., Quatrale A., Paradiso A. A new generation of MDR modulating agents with dual activity: P-gp inhibitor and iNOS inducer agents. Toxicol. in Vitro 2011, 25:222-230.
13. Di Pietro A., Conseil G., Perez-Victoria J.M., Dayan G., Baubichon-Cortay H., Trompier D., Steinfels E., Jault J.M., de Wet H., Maitrejean M., Comte G., Boumendjel A., Mariotte A.M., Dumontet C., McIntosh D.B., Goffeau A., Castanys S., Gamarro F., Barron D. Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell. Mol. Life Sci. 2002, 59:307-322.
14. Dietel M., Arps H., Lage H., Niendorf A. Membrane vesicle formation due to acquired mitoxantrone resistance in human gastric carcinoma cell line EPG85-257. Cancer Res. 1990, 50:6100-6106.
15. Erlund I. Review of flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, bioavailability, and epidemiology. Nutr. Res. 2004, 24:551-874.
16. Ferry D.R., Smith A., Malkhandi J., Fyfe D.W., deTakats 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. Clin. Cancer Res. 1996, 2:659-668.
17. Gibellini L., Pinti M., Nasi M., Montagna J.P., De Biasi S., Roat E., Bertoncelli L., Cooper E.L., Cossarizza A. Quercetin and cancer chemoprevention. Evid. Based Complement. Alternat. Med. 2011, 2011:591356.
18. 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). J. Nutr. 2006, 136:2715-2721.
19. Harwood M., Danielewska-Nikiel B., Borzelleca J.F., Flamm G.W., Williams G.M., Lines T.C. A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chem. Toxicol. 2007, 45:2179-2205.
20. Hou X.L., Takahashi K., Tanaka K., Tougou K., Qiu F., Komatsu K., Azuma J. Curcuma drugs and curcumin regulate the expression and function of P-gp in Caco-2 cells in completely opposite ways. Int. J. Pharm. 2008, 358:224-229.
21. Howells L.M., Britton R.G., Mazzoletti M., Greaves P., Broggini M., Brown K., Steward W.P., Gescher A.J., Sale S. Preclinical colorectal cancer chemopreventive efficacy and p53-modulating activity of 3',4',5'-trimethoxyflavonol, a quercetin analogue. Cancer Prev. Res. (Phila) 2010, 3:929-939.
22. Ishii K., Tanaka S., Kagami K., Henmi K., Toyoda H., Kaise T., Hirano T. Effects of naturally occurring polymethyoxyflavonoids on cell growth, p-glycoprotein function, cell cycle, and apoptosis of daunorubicin-resistant T lymphoblastoid leukemia cells. Cancer Invest. 2010, 28:220-229.
23. Ishisaka A., Ichikawa S., Sakakibara H., Piskula M.K., Nakamura T., Kato Y., Ito M., Miyamoto K., Tsuji A., Kawai Y., Terao J. Accumulation of orally administered quercetin in brain tissue and its antioxidative effects in rats. Free Radic. Biol. Med. 2011, 51:1329-1336.
24. Jia Y., Lin J., Mi Y., Zhang C. Quercetin attenuates cadmium-induced oxidative damage and apoptosis in granulosa cells from chicken ovarian follicles. Reprod Toxicol 2011, 31:477-485.
25. 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. Can. J. Physiol. Pharmacol. 2004, 82:1084-1090.
26. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
27. Lage H. An overview of cancer multidrug resistance. a still unsolved problem. Cell. Mol. Life Sci. 2008, 65:3145-3167.
28. Lee D.H., Szczepanski M., Lee Y.J. Role of Bax in quercetin-induced apoptosis in human prostate cancer cells. Biochem. Pharmacol. 2008, 75:2345-2355.
29. Lee W.J., Chen Y.R., Tseng T.H. Quercetin induces FasL-related apoptosis, in part, through promotion of histone H3 acetylation in human leukemia HL-60 cells. Oncol. Rep. 2011, 25:583-591.
30. Leslie E.M., Deeley R.G., Cole S.P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 2005, 204:216-237.
31. Liang W., Li X., Li C., Liao L., Gao B., Gan H., Yang Z., Chen X. Quercetin-mediated apoptosis via activation of the mitochondrial-dependent pathway in MG-63 osteosarcoma cells. Mol. Med. Report 2011, 4:1017-1023.
32. Mansilla S., Priebe W., Portugal J. Mitotic catastrophe results in cell death by caspase-dependent and caspase-independent mechanisms. Cell Cycle 2006, 5:53-60.
33. Minotti G., Menna P., Salvatorelli E., Cairo G., Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 2004, 56:185-229.
34. Morris M.E., Zhang S. Flavonoid-drug interactions: effects of flavonoids on ABC transporters. Life Sci. 2006, 78:2116-2130.
35. Murakami A., Ashida H., Terao J. Multitargeted cancer prevention by quercetin. Cancer Lett. 2008, 269:315-325.
36. Nabekura T., Kamiyama S., Kitagawa S. Effects of dietary chemopreventive phytochemicals on P-glycoprotein function. Biochem. Biophys. Res. Commun. 2005, 327:866-870.
37. Nagy H., Goda K., Fenyvesi F., Bacso Z., Szilasi M., Kappelmayer J., Lustyik G., Cianfriglia M., Szabo G. Distinct groups of multidrug resistance modulating agents are distinguished by competition of P-glycoprotein-specific antibodies. Biochem. Biophys. Res. Commun. 2004, 315:942-949.
38. Nguyen T.T., Tran E., Nguyen T.H., Do P.T., Huynh T.H., Huynh H. The role of activated MEK-ERK pathway in quercetin-induced growth inhibition and apoptosis in A549 lung cancer cells. Carcinogenesis 2004, 25:647-659.
39. Niu G., Yin S., Xie S., Li Y., Nie D., Ma L., Wang X., Wu Y. Quercetin induces apoptosis by activating caspase-3 and regulating Bcl-2 and cyclooxygenase-2 pathways in human HL-60 cells. Acta Biochim. Biophys. Sin. (Shanghai) 2011, 43:30-37.
40. Okamoto T. Safety of quercetin for clinical application (Review). Int. J. Mol. Med. 2005, 16:275-278.
41. Quan F., Pan C., Ma Q., Zhang S., Yan L. Reversal effect of resveratrol on multidrug resistance in KBv200 cell line. Biomed. Pharmacother. 2008, 62:622-629.
42. Roninson I.B., Broude E.V., Chang B.D. If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist. Updat. 2001, 4:303-313.
43. Rosner K., Ropke C., Pless V., Skovgaard G.L. Late type apoptosis and apoptosis free lethal effect of quercetin in human melanoma. Biosci. Biotechnol. Biochem. 2006, 70:2169-2177.
44. Ross J.A., Kasum C.M. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 2002, 22:19-34.
45. Salerno M., Garnier-Suillerot A. Kinetics of glutathione and daunorubicin efflux from multidrug resistance protein overexpressing small-cell lung cancer cells. Eur. J. Pharmacol. 2001, 421:1-9.
46. Scotto K.W. Transcriptional regulation of ABC drug transporters. Oncogene 2003, 22:7496-7511.
47. Seidel A., Hasmann M., Loser R., Bunge A., Schaefer B., Herzig I., Steidtmann K., Dietel M. Intracellular localization, vesicular accumulation and kinetics of daunorubicin in sensitive and multidrug-resistant gastric carcinoma EPG85-257 cells. Virchows Arch. 1995, 426:249-256.
48. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D., Warren J.T., Bokesch H., Kenney S., Boyd M.R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl Cancer Inst. 1990, 82:1107-1112.
49. Staedler D., Idrizi E., Kenzaoui B.H., Juillerat-Jeanneret L. Drug combinations with quercetin: doxorubicin plus quercetin in human breast cancer cells. Cancer Chemother. Pharmacol. 2011, 68:1161-1172.
50. Surh Y.J. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 2003, 3:768-780.
51. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., Gottesman M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 2006, 5:219-234.
52. Tan W.F., Lin L.P., Li M.H., Zhang Y.X., Tong Y.G., Xiao D., Ding J. Quercetin, a dietary-derived flavonoid, possesses antiangiogenic potential. Eur. J. Pharmacol. 2003, 459:255-262.
53. Vidya Priyadarsini R., Senthil Murugan R., Maitreyi S., Ramalingam K., Karunagaran D., Nagini S. The flavonoid quercetin induces cell cycle arrest and mitochondria-mediated apoptosis in human cervical cancer (HeLa) cells through p53 induction and NF-kappaB inhibition. Eur. J. Pharmacol. 2010, 649:84-91.
54. Wang E.J., Casciano C.N., Clement R.P., Johnson W.W. Cooperativity in the inhibition of P-glycoprotein-mediated daunorubicin transport: evidence for half-of-the-sites reactivity. Arch. Biochem. Biophys. 2000, 383:91-98.
55. 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). FEBS J. 2005, 272:4725-4740.
56. Xiao X., Shi D., Liu L., Wang J., Xie X., Kang T., Deng W. Quercetin suppresses cyclooxygenase-2 expression and angiogenesis through inactivation of P300 signaling. PLoS One 2011, 6:e22934.
57. Xu H.Z., Huang Y., Wu Y.L., Zhao Y., Xiao W.L., Lin Q.S., Sun H.D., Dai W., Chen G.Q. Pharicin A, a novel natural ent-kaurene diterpenoid, induces mitotic arrest and mitotic catastrophe of cancer cells by interfering with BubR1 function. Cell Cycle 2010, 9:2897-2907.
58. Yasuhara S., Zhu Y., Matsui T., Tipirneni N., Yasuhara Y., Kaneki M., Rosenzweig A., Martyn J.A. Comparison of comet assay, electron microscopy, and flow cytometry for detection of apoptosis. J. Histochem. Cytochem. 2003, 51:873-885.