Quercetin, a natural flavonoid interacts with DNA, arrests cell cycle and causes tumor regression by activating mitochondrial pathway of apoptosis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Srivastava, Shikha ^a   Somasagara, Ranganatha R ^a   Hegde, Mahesh ^a   Nishana, Mayilaadumveettil ^a   Tadi, Satish Kumar ^a   Srivastava, Mrinal ^a   Choudhary, Bibha ^b   Raghavan, Sathees C ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b Institute of Bioinformatics and Applied Biotechnology   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ELLAGIC ACID; QUERCETIN;

ANIMAL; APOPTOSIS; CELL CYCLE; CELL CYCLE CHECKPOINT; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; MOUSE; NEOPLASMS; SURVIVAL ANALYSIS; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ELLAGIC ACID; MICE; MITOCHONDRIA; NEOPLASMS; QUERCETIN; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84963976306     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24049     Document Type: Article

References (58)

1. Mertens-Talcott, S. U. & Percival, S. S. Ellagic acid and quercetin interact synergistically with resveratrol in the induction of apoptosis and cause transient cell cycle arrest in human leukemia cells. Cancer Lett 218, 141-151 (2005).
2. Mertens-Talcott, S. U., Talcott, S. T. & Percival, S. S. Low concentrations of quercetin and ellagic acid synergistically influence proliferation, cytotoxicity and apoptosis in MOLT-4 human leukemia cells. J Nutr 133, 2669-2674 (2003).
3. Haghiac, M. & Walle, T. Quercetin induces necrosis and apoptosis in SCC-9 oral cancer cells. Nutr Cancer 53, 220-231 (2005).
4. Senthilkumar, K., et al. Quercetin regulates insulin like growth factor signaling and induces intrinsic and extrinsic pathway mediated apoptosis in androgen independent prostate cancer cells (PC-3). Mol Cell Biochem 344, 173-184 (2010).
5. Zhang, H., et al. Antitumor activities of quercetin and quercetin-5' ,8-disulfonate in human colon and breast cancer cell lines. Food Chem Toxicol 50, 1589-1599 (2012).
6. Kim, G. N. & Jang, H. D. Protective mechanism of quercetin and rutin using glutathione metabolism on HO-induced oxidative stress in HepG2 cells. Ann N Y Acad Sci 1171, 530-537 (2009).
7. Robaszkiewicz, A., Balcerczyk, A. & Bartosz, G. Antioxidative and prooxidative effects of quercetin on A549 cells. Cell Biol Int 31, 1245-1250 (2007).
8. Brisdelli, F., Coccia, C., Cinque, B., Cifone, M. G. & Bozzi, A. Induction of apoptosis by quercetin: different response of human chronic myeloid (K562) and acute lymphoblastic (HSB-2) leukemia cells. Mol Cell Biochem 296, 137-149 (2007).
9. Yuan, Z., et al. Quercetin-induced apoptosis of HL-60 cells by reducing PI3K/Akt. Mol Biol Rep 39, 7785-7793 (2012).
10. Yoshida, M., Yamamoto, M. & Nikaido, T. Quercetin arrests human leukemic T-cells in late G1 phase of the cell cycle. Cancer Res 52, 6676-6681 (1992).
11. Richter, M., Ebermann, R. & Marian, B. Quercetin-induced apoptosis in colorectal tumor cells: possible role of EGF receptor signaling. Nutr Cancer 34, 88-99 (1999).
12. Choi, J. A., et al. Induction of cell cycle arrest and apoptosis in human breast cancer cells by quercetin. Int J Oncol 19, 837-844 (2001).
13. Lee, T. J., et al. Quercetin arrests G2/M phase and induces caspase-dependent cell death in U937 cells. Cancer Lett 240, 234-242 (2006).
14. Zhang, Q., Zhao, X. H. & Wang, Z. J. Flavones and flavonols exert cytotoxic effects on a human oesophageal adenocarcinoma cell line (OE33) by causing G2/M arrest and inducing apoptosis. Food Chem Toxicol 46, 2042-2053 (2008).
15. Pitchakarn, P., et al. Ellagic acid inhibits migration and invasion by prostate cancer cell lines. Asian Pac J Cancer Prev 14, 2859-2863 (2013).
16. Narayanan, B. A., Geoffroy, O., Willingham, M. C., Re, G. G. & Nixon, D. W. p53/p21(WAF1/CIP1) expression and its possible role in G1 arrest and apoptosis in ellagic acid treated cancer cells. Cancer Lett 136, 215-221 (1999).
17. Yang, F., et al. Combination of Quercetin and 2-Methoxyestradiol Enhances Inhibition of Human Prostate Cancer LNCaP and PC-3 Cells Xenograft Tumor Growth. Plos One 10, e0128277 (2015).
18. Ravishankar, D., et al. Exploring quercetin and luteolin derivatives as antiangiogenic agents. Eur J Med Chem 97, 259-274 (2015).
19. Wang, G., Zhang, J., Liu, L., Sharma, S. & Dong, Q. Quercetin potentiates doxorubicin mediated antitumor effects against liver cancer through p53/Bcl-xl. Plos One 7, e51764 (2012).
20. Nessa, M. U., Beale, P., Chan, C., Yu, J. Q. & Huq, F. Synergism from combinations of cisplatin and oxaliplatin with quercetin and thymoquinone in human ovarian tumour models. Anticancer Res 31, 3789-3797 (2011).
21. Akagi, K., et al. Modulating effects of ellagic acid, vanillin and quercetin in a rat medium term multi-organ carcinogenesis model. Cancer Lett 94, 113-121 (1995).
22. Srivastava, M. R. S. DNA double-strand break repair inhibitors as cancer therapeutics. Chem Biol 22, 17-29 (2015).
23. Somasagara, R. R., et al. Extracts of strawberry fruits induce intrinsic pathway of apoptosis in breast cancer cells and inhibits tumor progression in mice. Plos One 7, e47021 (2012).
24. Srivastava, M., et al. Sapodilla plum (Achras sapota) induces apoptosis in cancer cell lines and inhibits tumor progression in mice. Sci Rep 4, 6147 (2014).
25. Chiruvella, K. K., et al. Methyl angolensate, a natural tetranortriterpenoid induces intrinsic apoptotic pathway in leukemic cells. FEBS Lett 582, 4066-4076 (2008).
26. Chiruvella, K. K., Panjamurthy, K., Choudhary, B., Joy, O. & Raghavan, S. C. Methyl angolensate from callus of Indian redwood induces cytotoxicity in human breast cancer cells. Int J Biomed Sci 6, 182-194 (2010).
27. Chiruvella, K. K. & Raghavan, S. C. A natural compound, methyl angolensate, induces mitochondrial pathway of apoptosis in Daudi cells. Invest New Drugs 29, 583-592 (2011).
28. Sharma, S., et al. A novel DNA intercalator, 8-methoxy pyrimido[4' ,5' :4,5]thieno (2,3-b)quinoline-4(3H)-one induces apoptosis in cancer cells, inhibits the tumor progression and enhances lifespan in mice with tumor. Mol Carcinog 52, 413-425 (2013).
29. Shahabuddin, M. S., Nambiar, M., Choudhary, B., Advirao, G. M. & Raghavan, S. C. A novel DNA intercalator, butylaminopyrimido[ 4' ,5' :4,5]selenolo(2,3-b)quinoline, induces cell cycle arrest and apoptosis in leukemic cells. Invest New Drugs 28, 35-48 (2010).
30. John, F., et al. Pluronic copolymer encapsulated SCR7 as a potential anticancer agent. Faraday Discuss 177, 155-161 (2015).
31. Srivastava, M., et al. An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression. Cell 151, 1474-1487 (2012).
32. Hegde, M., et al. Novel levamisole derivative induces extrinsic pathway of apoptosis in cancer cells and inhibits tumor progression in mice. Plos One 7, e43632 (2012).
33. Kavitha, C. V., et al. Propyl-2-(8-(3,4-difluorobenzyl)-2' ,5' -dioxo-8-azaspiro[bicyclo[3.2.1] octane-3,4' -imidazolidine]-1' -yl) acetate induces apoptosis in human leukemia cells through mitochondrial pathway following cell cycle arrest. Plos One 8, e69103 (2013).
34. Kavitha, C. V., et al. Novel derivatives of spirohydantoin induce growth inhibition followed by apoptosis in leukemia cells. Biochem Pharmacol 77, 348-363 (2009).
35. Overby, A., Zhao, C. M. & Chen, D. Plant phytochemicals: potential anticancer agents against gastric cancer. Curr Opin Pharmacol 19C, 6-10 (2014).
36. Khanduja, K. L., Gandhi, R. K., Pathania, V. & Syal, N. Prevention of N-nitrosodiethylamine-induced lung tumorigenesis by ellagic acid and quercetin in mice. Food Chem Toxicol 37, 313-318 (1999).
37. Umesalma, S., Nagendraprabhu, P. & Sudhandiran, G. Ellagic acid inhibits proliferation and induced apoptosis via the Akt signaling pathway in HCT-15 colon adenocarcinoma cells. Mol Cell Biochem 399, 303-313 (2014).
38. Bishayee, K., et al. Quercetin induces cytochrome-c release and ROS accumulation to promote apoptosis and arrest the cell cycle in G2/M, in cervical carcinoma: signal cascade and drug-DNA interaction. Cell Prolif 46, 153-163 (2013).
39. Borska, S., et al. In vitro effect of quercetin on human gastric carcinoma: targeting cancer cells death and MDR. Food Chem Toxicol 50, 3375-3383 (2012).
40. Huang, S. L., Hsu, C. L. & Yen, G. C. Growth inhibitory effect of quercetin on SW 872 human liposarcoma cells. Life Sci 79, 203-209 (2006).
41. Wenzel, U., Herzog, A., Kuntz, S. & Daniel, H. Protein expression profiling identifies molecular targets of quercetin as a major dietary flavonoid in human colon cancer cells. Proteomics 4, 2160-2174 (2004).
42. Huang, Y. T., et al. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis-associated properties in A431 cells overexpressing epidermal growth factor receptor. Br J Pharmacol 128, 999-1010 (1999).
43. Yoshida, M., et al. The effect of quercetin on cell cycle progression and growth of human gastric cancer cells. FEBS Lett 260, 10-13 (1990).
44. Son, Y. O., et al. Selective effects of quercetin on the cell growth and antioxidant defense system in normal versus transformed mouse hepatic cell lines. Eur J Pharmacol 502, 195-204 (2004).
45. Pratheeshkumar, P., et al. Quercetin inhibits angiogenesis mediated human prostate tumor growth by targeting VEGFR-2 regulated AKT/mTOR/P70S6K signaling pathways. Plos One 7, e47516 (2012).
46. Noaman, E., Badr El-Din, N. K., Bibars, M. A., Abou Mossallam, A. A. & Ghoneum, M. Antioxidant potential by arabinoxylan rice bran, MGN-3/biobran, represents a mechanism for its oncostatic effect against murine solid Ehrlich carcinoma. Cancer Lett 268, 348-359 (2008).
47. Gekeler, V., Epple, J., Kleymann, G. & Probst, H. Selective and synchronous activation of early-S-phase replicons of Ehrlich ascites cells. Mol Cell Biol 13, 5020-5033 (1993).
48. Kumar, A., et al. Antiangiogenic and antiproliferative effects of substituted-1,3,4-oxadiazole derivatives is mediated by down regulation of VEGF and inhibition of translocation of HIF-1alpha in Ehrlich ascites tumor cells. Cancer Chemother Pharmacol 64, 1221-1233 (2009).
49. Vidya Priyadarsini, R., et al. 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 649, 84-91 (2010).
50. Hengartner, M. O. The biochemistry of apoptosis. Nature 407, 770-776 (2000).
51. Chan, S. T., Yang, N. C., Huang, C. S., Liao, J. W. & Yeh, S. L. Quercetin enhances the antitumor activity of trichostatin A through upregulation of p53 protein expression in vitro and in vivo. Plos One 8, e54255 (2013).
52. Ko, C. C., et al. Chemical proteomics identifies heterogeneous nuclear ribonucleoprotein (hnRNP) A1 as the molecular target of quercetin in its anti-cancer effects in PC-3 cells. J Biol Chem 289, 22078-22089 (2014).
53. Slusarz, A., et al. Common botanical compounds inhibit the hedgehog signaling pathway in prostate cancer. Cancer Res 70, 3382-3390 (2010).
54. 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. Mol Cancer Therapeut 6, 2591-2599 (2007).
55. Boly, R., et al. Quercetin inhibits a large panel of kinases implicated in cancer cell biology. Int J Oncol 38, 833-842 (2011).
56. Freimoser, F. M., Jakob, C. A., Aebi, M. & Tuor, U. The MTT [3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide] assay is a fast and reliable method for colorimetric determination of fungal cell densities. Appl Environ Microbiol 65, 3727-3729 (1999).
57. Sharma, S., Choudhary, B. & Raghavan, S. C. Efficiency of nonhomologous DNA end joining varies among somatic tissues, despite similarity in mechanism. Cell Mol Life Sci 68, 661-676 (2011).
58. Sahu, U., et al. A Novel Anticancer Agent, 8-Methoxypyrimido[4' ,5' :4,5]thieno(2,3-) Quinoline-4(3H)-One Induces Neuro 2a Neuroblastoma Cell Death through p53-Dependent, Caspase-Dependent and -Independent Apoptotic Pathways. Plos One 8, e66430 (2013).