The role of quercetin and vitamin c in NRF2-dependent oxidative stress production in breast cancer cells

Oncology Letters

Volumn 13, Issue 3, 2017, Pages 1965-1973

  Mostafavi Pour, Zohreh ^a,b   Ramezani, Fatemeh ^c   Keshavarzi, Fatemeh ^a   Samadi, Nasser ^d  

^a MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Nrf2; Quercetin; Reactive oxygen species; Vitamin C

Indexed keywords

2,6 DICHLOROPHENOLINDOPHENOL; 5,5' DITHIOBIS(2 NITROBENZOIC ACID); ASCORBIC ACID; DICHLORODIHYDROFLUORESCEIN DIACETATE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEME OXYGENASE 1; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; TRANSCRIPTION FACTOR NRF2;

A-549 CELL LINE; ARTICLE; BREAST CANCER CELL LINE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENZYME ACTIVITY; FLUOROMETRY; HUMAN; HUMAN CELL; IC50; MCF-7 CELL LINE; MDA-MB CELL LINE; MICROSOME; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING;

EID: 85011932294     PISSN: 17921074     EISSN: 17921082     Source Type: Journal    
DOI: 10.3892/ol.2017.5619     Document Type: Article

References (47)

1. Ramos S: Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. J Nutr Biochem 18: 427-442, 2007.
2. No JH, Kim YB and Song YS: Targeting nrf2 signaling to combat chemoresistance. J Cancer Prev 19: 111-117, 2014.
3. Wu T, Harder BG, Wong PK, Lang JE and Zhang DD: Oxidative stress, mammospheres and Nrf2-new implication for breast cancer therapy? Mol Carcinog 54: 1494-1502, 2015.
4. Jaramillo MC and Zhang DD: The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27: 2179-2191, 2013.
5. Kensler TW, Wakabayashi N and Biswal S: Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
6. Foygel K, Sekar TV and Paulmurugan R: Monitoring the antioxidant mediated chemosensitization and ARE-signaling in triple negative breast cancer therapy. PloS One 10: e0141913, 2015.
7. Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, Chen W, Yi X, Zheng W, Wondrak GT, et al: Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 29: 1235-1243, 2008.
8. Amadori D, Frassineti G, Zoli W, Milandri C, Serra P, Tienghi A, Ravaioli A, Gentile A and Salzano E: Doxorubicin and paclitaxel (sequential combination) in the treatment of advanced breast cancer. Oncology (Williston Park) 11: (4 Suppl 3) 30-33, 1997.
9. Danesi R, Conte PF and Del Tacca M: Pharmacokinetic optimisation of treatment schedules for anthracyclines and paclitaxel in patients with cancer. Clin Pharmacokinet 37: 195-211, 1999.
10. Ibrahim T, Fabbri M, Frassineti GL, Zoli W, Monti M, Ricotti L and Amadori D: Doxorubicin, paclitaxel and gemcitabine: A Phase I study of a new sequential treatment in stage III B-IV breast cancer. J Chemother 15: 488-494, 2003.
11. Chou TC: Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-681, 2006.
12. Lee KW, Lee HJ, Surh YJ and Lee CY: Vitamin C and cancer chemoprevention: Reappraisal. Am J Clin Nutr 78: 1074-1078, 2003.
13. Zielinski CC: Gemcitabine, anthracycline, and taxane combinations for advanced breast cancer. Oncology (Williston Park) 17: (12 Suppl 14) 36-40, 2003.
14. Chao MW, Lai MJ, Liou JP, Chang YL, Wang JC, Pan SL and Teng CM: The synergic effect of vincristine and vorinostat in leukemia in vitro and in vivo. J Hematol Oncol 8: 82, 2015.
15. Weiss RB, Woolf SH, Demakos E, Holland JF, Berry DA, Falkson G, Cirrincione CT, Robbins A, Bothun S, Henderson IC, et al: Natural history of more than 20 years of node-positive primary breast carcinoma treated with cyclophosphamide, methotrexate, and fluorouracil-based adjuvant chemotherapy: A study by the cancer and leukemia group B. J Clin Oncol 21: 1825-1835, 2003.
16. Tarumoto T, Nagai T, Ohmine K, Miyoshi T, Nakamura M, Kondo T, Mitsugi K, Nakano S, Muroi K, Komatsu N and Ozawa K: Ascorbic acid restores sensitivity to imatinib via suppression of Nrf2-dependent gene expression in the imatinib-resistant cell line. Exp Hematol 32: 375-381, 2004.
17. Khanduja KL, Gandhi RK, Pathania V and Syal N: Prevention of N-nitrosodiethylamine-induced lung tumorigenesis by ellagic acid and quercetin in mice. Food Chem Toxicol 37: 313-318, 1999.
18. Saw CL, Guo Y, Yang AY, Paredes-Gonzalez X, Ramirez C, Pung D and Kong AN: The berry constituents quercetin, kaemp- ferol, and pterostilbene synergistically attenuate reactive oxygen species: Involvement of the Nrf2-ARE signaling pathway. Food Chem Toxicol 72: 303-311, 2014.
19. Borska S, Chmielewska M, Wysocka T, Drag-Zalesinska M, Zabel M and Dziegiel P: In vitro effect of quercetin on human gastric carcinoma: Targeting cancer cells death and MDR. Food Chem Toxicol 50: 3375-3383, 2012.
20. Granado-Serrano AB, Martin MA, Bravo L, Goya L and 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 136: 2715-2721, 2006.
21. Li N, Sun C, Zhou B, Xing H, Ma D, Chen G and Weng D: Low concentration of quercetin antagonizes the cytotoxic effects of anti-neoplastic drugs in ovarian cancer. PloS One 9: e100314, 2014.
22. Robaszkiewicz A, Balcerczyk A and Bartosz G: Antioxidative and prooxidative effects of quercetin on A549 cells. Cell Biol Int 31: 1245-1250, 2007.
23. Samuel T, Fadlalla K, Mosley L, Katkoori V, Turner T and Manne U: Dual-mode interaction between quercetin and DNA-damaging drugs in cancer cells. Anticancer Res 32: 61-71, 2012.
24. Granado-Serrano AB, Martin MA, Bravo L, Goya L and Ramos S: Quercetin modulates Nrf2 and glutathione-related defenses in HepG2 cells: Involvement of p38. Chem Biol Interact 195: 154-164, 2012.
25. Pfaffl MW: Quantification strategies in real-time PCR. A-Z of quantitative PCR 3: 87-112, 2004.
26. Sabzichi M, Samadi N, Mohammadian J, Hamishehkar H, Akbarzadeh M and Molavi O: Sustained release of melatonin: A novel approach in elevating efficacy of tamoxifen in breast cancer treatment. Colloids Surf B Biointerfaces 145: 64-71, 2016.
27. Fecondo JV and Augusteyn RC: Superoxide dismutase, catalase and glutathione peroxidase in the human cataractous lens. Exp Eye Res 36: 15-23, 1983.
28. Maiani G, Mobarhan S, Nicastro A, Virgili F, Scaccini C and Ferro-Luzzi A: Determination of glutathione reductase activity in erythrocytes and whole blood as an indicator of riboflavin nutrition. Acta Vitaminol Enzymol 5: 171-178, 1982 (In Italian).
29. Ellman GL: Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77, 1959.
30. Furfaro A, Traverso N, Domenicotti C, Piras S, Moretta L, Marinari UM, Pronzato MA and Nitti M: The Nrf2/HO-1 axis in cancer cell growth and chemoresistance. Oxid Med Cell Longev 2016: 1958174, 2016.
31. van der Wijst MG, Brown R and Rots MG: Nrf2, the master redox switch: The Achilles' heel of ovarian cancer? Biochim Biophys Acta 1846: 494-509, 2014.
32. Liu KC, Yen CY, Wu RS, Yang JS, Lu HF, Lu KW, Lo C, Chen HY, Tang NY, Wu CC and Chung JG: The roles of endoplasmic reticulum stress and mitochondrial apoptotic signaling pathway in quercetin-mediated cell death of human prostate cancer PC-3 cells. Environ Toxicol 29: 428-439, 2014.
33. Lee WJ, Hsiao M, Chang JL, Yang SF, Tseng TH, Cheng CW, Chow Jm, Lin KH, Lin Yw, Liu CC, et al: Quercetin induces mitochondrial-derived apoptosis via reactive oxygen species-mediated ERK activation in HL-60 leukemia cells and xenograft. Arch Toxicol 89: 1103-1117, 2015.
34. Bournival J, Francoeur MA, Renaud J and Martinoli MG: Quercetin and sesamin protect neuronal PC12 cells from high-glucose-induced oxidation, nitrosative stress, and apoptosis. Rejuvenation Res 15: 322-333, 2012.
35. Bouayed J and Bohn T: Exogenous antioxidants-double-edged swords in cellular redox state: Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid Med Cell Longev 3: 228-237, 2010.
36. Carr AC, Vissers MC and Cook JS: The effect of intravenous vitamin C on cancer-and chemotherapy-related fatigue and quality of life. Front Oncol 4: 283, 2014.
37. Chen MF, Yang CM, Su CM and Hu ML: Vitamin C protects against cisplatin-induced nephrotoxicity and damage without reducing its effectiveness in C57BL/6 mice xenografted with Lewis lung carcinoma. Nutr Cancer 66: 1085-1091, 2014.
38. Wang X, Ye XL Liu R, Chen HL, Bai H, Liang X, Zhang XD, Wang Z, Li WL and Hai CX: Antioxidant activities of oleanolic acid in vitro: Possible role of Nrf2 and MAP kinases. Chem Biol Interact 184: 328-337, 2010.
39. Ding M, Zhao J, Bowman L, Lu Y and Shi X: Inhibition of AP-1 and MAPK signaling and activation of Nrf2/ARE pathway by quercitrin. Int J Oncol 36: 59-67, 2010.
40. Chun KS, Kundu J, Kundu JK and Surh YJ: Targeting Nrf2-Keap1 signaling for chemoprevention of skin carcinogenesis with bioactive phytochemicals. Toxicol Lett 229: 73-84, 2014.
41. Minaei A, Sabzichi M, Ramezani F, Hamishehkar H and Samadi N: Co-delivery with nano-quercetin enhances doxorubicin-mediated cytotoxicity against MCF-7 cells. Mol Biol Rep 43: 99-105, 2016.
42. Ren D, Villeneuve NF, Jiang T, Wu T, Lau A, Toppin HA and Zhang DD: Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc Natl Acad Sci USA 108: 1433-1438, 2011.
43. Wagner AE, Ernst I, Iori R, Desel C and Rimbach G: Sulfora- phane but not ascorbigen, indole-3-carbinole and ascorbic acid activates the transcription factor Nrf2 and induces phase-2 and antioxidant enzymes in human keratinocytes in culture. Exp Dermatol 19: 137-144, 2010.
44. Scharf G, Prustomersky S, Knasmuller S, Schulte-Hermann R and Huber WW: Enhancement of glutathione and g-glutamylcysteine synthetase, the rate limiting enzyme of glutathione synthesis, by chemoprotective plant-derived food and beverage components in the human hepatoma cell line HepG2. Nutr Cancer 45: 74-83, 2003.
45. Goldring CE, Kitteringham NR, Elsby R, Randle LE, Clement YN, Williams DP, McMahon M, Hayes JD, Itoh K, Yamamoto M and Park BK: Activation of hepatic Nrf2 in vivo by acetaminophen in CD-1 mice. Hepatology 39: 1267-1276, 2004.
46. Hanneken A, Lin FF, Johnson J and Maher P: Flavonoids protect human retinal pigment epithelial cells from oxidative-stress-induced death. Invest Ophthalmol Vis Sci 47: 3164-3177, 2006.
47. Parrow NL, Leshin JA and Levine M: Parenteral ascorbate as a cancer therapeutic: A reassessment based on pharmacokinetics. Antioxid Redox Signal 19: 2141-2156, 2013.