Differential cytotoxic activity of Quercetin on colonic cancer cells depends on ROS generation through COX-2 expression

Food and Chemical Toxicology

Volumn 106, Issue , 2017, Pages 92-106

  Raja, Subramaniya Bharathi ^a   Rajendiran, Vijayabharathi ^a   Kasinathan, Nirmal Kumar ^a   Amrithalakshmi, A P ^a   Venkatabalasubramanian, Sivaramakrishnan ^b   Murali, Malliga Raman ^c   Devaraj, Halagowder ^a   Devaraj, Sivasithamparam Niranjali ^a  

^a UNIVERSITY OF MADRAS   (India)

^b SASTRA UNIVERSITY   (India)

^c UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Colorectal cancer; COX 2; Cytotoxicity; NFkB; Quercetin; Reactive oxygen species

Indexed keywords

CASPASE 3; CYCLIN D1; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; QUERCETIN; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE; CELL SURVIVAL; COLON CANCER CELL LINE; COLORECTAL CANCER; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTESTINE EPITHELIUM CELL; MOLECULAR DOCKING; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; CELL PROLIFERATION; COLON TUMOR; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; PATHOPHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; HUMANS; NF-KAPPA B; QUERCETIN; REACTIVE OXYGEN SPECIES;

EID: 85019904290     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2017.05.006     Document Type: Article

References (59)

1. AI-Fayez, M., Cai, H., Tunstall, R., Steward, W.P., Gescher, A.J., Differential modulation of cyclooxygenase-mediated prostaglandin production by the putative cancer chemopreventive flavonoids tricin, apigenin and quercetin. Cancer Chemothe Pharmacol. 58 (2006), 816–825.
2. AI-Fayez, M., Cai, H., Tunstall, R., Steward, W.P., Gescher, A.J., Differential modulation of cyclooxygenase-mediated prostaglandin production by the putative cancer chemopreventive flavonoids tricin, apigenin and quercetin. Cancer Chemother. Pharmacol. 58 (2006), 816–825.
3. Arber, N., Levin, B., Chemoprevention of colorectal cancer: ready for routine use?. Recent Results Cancer Res. 166 (2005), 213–230.
4. Arthur, Janelle C., Jobin, Christian, The complex interplay between inflammation, the microbiota and colorectal cancer. Gut Microbes 4:3 (2013), 253–258.
5. Avila, M.A., Velasco, J.A., Cansado, J., Notario, V., Quercetin mediates the down-regulation of mutant p53 in the human breast cancer cell line MDA-MB468. Cancer Res. 54 (1994), 2424–2428.
6. Baldwin, A.S., Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J. Clin. Invest. 107:3 (2001), 241–246.
7. Buchanan, F.G., Wang, D., Bargiacchi, F., DuBois, R.N., Prostaglandin E2 regulates cell migration via the intracellular activation of the epidermal growth factor receptor. J. Biol. Chem. 278 (2003), 35451–35457.
8. Casagrande, F., Darbon, J.M., Effects of structurally related flavonoids on cell cycle progression of human melanoma cells: regulation of cyclin-dependent kinases CDK2 and CDK1. Biochem. Pharmacol. 61 (2001), 1205–1215.
9. Choi, J.A., Kim, J.Y., Lee, J.Y., Kang, C.M., Kwon, H.J., Yoo, Y.D., Kim, T.W., Lee, Y.S., Lee, S.J., Induction of cell cycle arrest and apoptosis in human breast cancer cells by quercetin. Int. J. Oncol. 19 (2001), 837–844.
10. Cole, S.P., Rapid chemosensitivity testing of human lung tumor cells using the MTT assay. Cancer Chemother. Pharmacol. 17:3 (1986), 259–263.
11. Diehl, J.A., Cycling to cancer with cyclin D1. Cancer Biol. Ther. 1:3 (2002), 226–231.
12. Du, G., Lin, H., Wang, M., Zhang, S., Wu, X., Lu, L., et al. Quercetin greatly improved therapeutic index of doxorubicin against 4T1 breast cancer by its opposing effects on HIF-1a in tumor and normal cells. Cancer Chemother. Pharmacol. 65 (2010), 277–287.
13. Egert, S., Wolffram, S., Bosy-Westphal, A., Boesch-Saadatmandi, C., Wagner, A.E., Frank, J., Rimbach, G., Mueller, M.J., Daily Quercetin supplementation dose-dependently increases plasma Quercetin concentrations in healthy humans. J. Nutr. 138:9 (2008), 1615–1621.
14. Finkel, T., Signal transduction by reactive oxygen species. J. Cell Biol. 194 (2011), 7–15.
15. Giles, R.H., van Es, J.H., Clevers, H., Caught up in a Wnt storm: wntsignaling in cancer. Biochem. Biophys. Acta 1653 (2003), 1–24.
16. Gorlick, R., Bertino, J.R., Drug resistance in colon cancer. Semin. Oncol. 26:6 (1999), 606–611.
17. 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. 136 (2006), 2715–2721.
18. Granado-Serrano, A.B., Martín, M.A., Bravo, L., Goya, L., Ramos, S., Quercetin modulates NF-kappa B and AP-1/JNK pathways to induce cell death in human hepatoma cells. Nutr. Cancer 62:3 (2010), 390–401.
19. Gupta, R.A., Dubois, R.N., Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer 1 (2001), 11–21.
20. Han, J.A., Cyclooxygenase-2 promotes cell proliferation, migration and invasion in U2OS human osteosarcoma cells. Exp. Mol. Med. 39 (2007), 469–476.
21. Hockenberry, D., Defining apoptosis. Am. J. Pathol. 146 (1995), 16–19.
22. Hosokawa, N., Hosokawa, Y., Sakai, T., Yoshida, M., Marui, N., Nishino, H., Kawai, K., Aoike, A., Inhibitory effect of quercetin on the synthesis of a possibly cell-cycle-related 17-kDa protein in human colon cancer cells. Int. J. Cancer 45 (1990), 1119–1124.
23. Jemal, A., Siegel, R., Ward, E., Murray, T., Xu, J., Thun, M.J., Cancer statistics. CA Cancer J. Clin. 57 (2007), 43–66.
24. Kandaswami, C., Lee, L.T., Lee, P.P., Hwang, J.J., Ke, F.C., Huang, Y.T., Lee, M.T., The antitumor activities of flavonoids. In Vivo 19 (2005), 895–909.
25. Kasinathan, N.K., Subramaniya, B.R., Pandian, I., Sivasithamparam, N.D., Aeglemarmelos fruit extract abates dextran sodium sulfate induced acute colitis in mice: repression of pro-inflammatory cytokines during colonic inflammation. Biomed. Prev. Nutr. 4:2 (2014), 307–317.
26. Ke, J., Long, X., Liu, Y., Zhang, Y.F., Li, J., Fang, W., Meng, Q.G., Role of NF-kappaB in TNF-alpha-induced COX-2 expression in synovial fibroblasts from human TMJ. J. Dent. Res. 86:4 (2007), 363–367.
27. Kim, Hyeong-Jin, Kim, Sang-Ki, Kim, Byeong-Soo, Lee, Seung-Ho, Park, Young-Seok, Park, Byung-Kwon, Kim, So-Jung, Kim, Jin, Choi, Changsun, Kim, Jong-Suk, Cho, Sung-Dae, Jung, Ji-Won, Roh, X Kyong-Hwan, Kang, Kyung-Sun, Jung, Ji-Youn, Apoptotic effect of quercetin on HT-29 colon cancer cells via the AMPK signaling pathway. J. Agric. Food Chem. 58 (1998), 8643–8650.
28. Kinzler, K.W., Vogelstein, B., Lessons from hereditary colorectal cancer. Cell 87 (1996), 159–170.
29. Kumar, K.N., Raja, S.B., Vidhya, N., Devaraj, S.N., Ellagic acid modulates antioxidant status, ornithine decarboxylase expression, and aberrant crypt foci progression in 1,2-dimethylhydrazine-instigated colon preneoplastic lesions in rats. J. Agric. Food Chem. 60 (2012), 3665–3672.
30. Lee, E.J., Choi, E.M., Kim, S.R., Park, J.H., Kim, H., Ha, K.S., Kim, Y.M., Kim, S.S., Choe, M., Kim, J.I., Han, J.A., Cyclooxygenase-2 promotes cell proliferation, migration and invasion in U2OS human osteosarcoma cells. Exp. Mol. Med. 39 (2007), 469–476.
31. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
32. Mangan, D.F., Wahl, S.M., Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines. J. Immunol. 147:10 (1991), 3408–3412.
33. Mariani, Francesco, Sena, Paola, Roncucci, Luca, Inflammatory pathways in the early steps of colorectal cancer development. World J. Gastroenterol. 20:29 (2014), 9716–9731.
34. Moriasi, Cate, Subramaniam, Dharmalingam, Awasthi, Shanjana, Anant, Shrikant, Ramalingam, Satish, Prevention of colitis-associated cancer: natural compounds that target the Il-6 soluble receptor. Anticancer Agents Med. Chem. 12:10 (2012), 1221–1238.
35. O'Leary, K.A., de Pascual-Tereasa, S., Needs, P.W., Bao, Y.P., O'Brien, N.M., Williamson, G., Effect of flavonoids and vitamin E on cyclooxygenase-2 (COX-2) transcription. Mutat. Res. 551 (2004), 245–254.
36. Oshima, M., Dinchuk, J.E., Kargman, S.L., Oshima, H., Hancock, B., Kwong, E., Trzaskos, J.M., Evans, J.F., Taketo, M.M., Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87 (1996), 803–809.
37. Park, M.H., Min do, S., Quercetin-induced downregulation of phospholipase D1 inhibits proliferation and invasion in U87 glioma cells. Biochem. Biophys. Res. Commun. 412 (2011), 710–715.
38. Ramos, S., Cancer chemoprevention and chemotherapy: dietary polyphenols and signaling pathways. Mol. Nutr. Food. Res. 52 (2008), 507–526.
39. Ranelletti, F.O., Maggiano, N., Serra, F.G., Ricci, R., Larocca, L.M., Lanza, P., Scambia, G., Fattorossi, A., Capelli, A., Piantelli, M., Quercetin inhibits p21-RAS expression in human colon cancer cell lines and in primary colorectal tumors. Int. J. Cancer 85 (2000), 438–445.
40. Reuter, Simone, Gupta, Subash C., Chaturvedi, Madan M., Aggarwal, Bharat B., Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 49:11 (2010), 1603–1616.
41. Rodrigues, N.R., Rowan, A., Smith, M.E., Kerr, I.B., Bodmer, W.F., Gannon, J.V., Lane, D.P., p53 mutations in colorectal cancer. Proc. Natl. Acad. Sci. 87 (1990), 7555–7559.
42. Ruiz, P.A., Braune, A., Hölzlwimmer, G., Quintanilla-Fend, L., Haller, D., Quercetin inhibits TNF-induced NF-kappaB transcription factor recruitment to pro-inflammatory gene promoters in murine intestinal epithelial cells. J. Nutr. 137:5 (2007), 1208–1215.
43. Rupnarain, C., Dlamini, Z., Naicker, S., Bhoola, K., Coloncancer: genomics and apoptotic events. BiolChem. 385 (2004), 449–464.
44. Russo, G.L., Ins and outs of dietary phytochemicals in cancer chemoprevention. Biochem. Pharmacol. 74 (2007), 533–544.
45. Samowitz, W.S., Slattery, M., Missense mismatch repair gene alterations, microsatellite instability and hereditary nonpolyposis colorectal cancer. J. Clin. Oncol. 20 (2002), 1203–1208.
46. Sebolt-Leopold, J.S., Dudley, D.T., Herrera, R., Van Becelaere, K., Wiland, A., Gowan, R.C., Tecle, H., Barrett, S.D., Bridges, A., Przybranowski, S., Leopold, W.R., Saltiel, A.R., Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat. Med. 5 (1999), 736–737.
47. Shan, B.E., Wang, M.X., Li, R.Q., Quercetin inhibits human SW480 colon cancer growth in association with inhibition of cyclin D1 and survivin expression through Wnt/beta-catenin signaling pathway. Cancer Invest. 27 (2009), 604–612.
48. Shao, Z.M., Wu, J., Shen, Z.Z., Barsky, S.H., Genistein exerts multiple suppressive effects on human breast carcinoma cells. Cancer Res. 58 (1998), 4851–4857.
49. Sharma, M.D., Ghosh, R., Patra, A., Hazra, B., Synthesis and antiproliferative activity of some novel derivatives of diospyrin, a plant-derived naphthoquinonoid. Bioorg Med. Chem. 15 (2007), 3672–3677.
50. Shintani, M., Okazaki, A., Masuda, T., Kawada, M., Ishizuka, M., Doki, Y., Weinstein, I.B., Imoto, M., Overexpression of cyclin DI contributes to malignant properties of esophagealtumor cells by increasing VEGF production and decreasing Fas expression. Anticancer Res. 22:2A (2002), 639–644.
51. Subramaniya, B.R., Srinivasan, G., Mohammed Sadullah, S.S., Davis, N., Baddi Reddi Subhadara, L., Devaraj, H., Devaraj, S.N., Apoptosis inducing effect of Plumbagin on colonic cancer cells depends on expression of COX-2. PLoS One, 6(4), 2011, e18695.
52. Thomasset, S.C., Berry, D.P., Garcea, G., Marczylo, T., Steward, W.P., Gescher, A.J., Dietary polyphenolic phytochemicals promising cancer chemopreventive agents in humans? A review of their clinical properties. Int. J. Cancer 120 (2007), 451–458.
53. Watson, W.H., Cai, J., Jones, D.P., Diet and apoptosis. Annu. Rev. Nutr. 20 (1998), 485–505.
54. Wojtala, A., Bonora, M., Malinska, D., Pinton, P., Duszynski, J., Wieckowski, M.R., Methods to monitor ROS production by fluorescence microscopy and fluorometry. Methods Enzymol. 542 (2014), 243–262.
55. Yang, L., Liu, Y., Wang, M., Qian, Y., Dong, X., Gu, H., Wang, H., Guo, S., Hisamitsu, T., Quercetin-induced apoptosis of HT-29 colon cancer cells via inhibition of the Akt-CSN6-Myc signaling axis. Mol. Med. Rep. 14:5 (2016 Nov), 4559–4566.
56. Yoshida, M., Sakai, T., Hosokawa, N., Marui, N., Matsumoto, K., Fujioka, A., Nishino, H., Aoike, A., The effect of quercetin on cell cycle progression and growth of human gastric cancer cells. FEBS Lett. 260 (1990), 10–13.
57. Yoshida, M., Yamamoto, M., Nikaido, T., Quercetin arrests human leukemic T-cells in late G1 phase of the cell cycle. Cancer Res. 52 (1992), 6676–6681.
58. Zhang, X.A., Zhang, S., Yin, Q., Zhang, J., Quercetin induces human colon cancer cells apoptosis by inhibiting the nuclear factor-kappa B pathway. Apr-Jun Pharmacogn. Mag. 11:42 (2015), 404–409.
59. Zhou, J.R., Mukherjee, P., Gugger, E.T., Tanaka, T., Blackburn, G.L., Clinton, S.K., Inhibition of murine bladder tumorigenesis by soy isoflavones via alterations in the cell cycle, apoptosis, and angiogenesis. Cancer Res. 58 (1998), 5231–5238.